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PMID: 18480280 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Latent stem and progenitor cells in the hippocampus are activated by neural excitation.

Walker TL, White A, Black DM, Wallace RH, Sah P, Bartlett PF

Abstract

The regulated production of neurons in the hippocampus throughout life underpins important brain functions such as learning and memory. Surprisingly, however, studies have so far failed to identify a resident hippocampal stem cell capable of providing the renewable source of these neurons. Here, we report that depolarizing levels of KCl produce a threefold increase in the number of neurospheres generated from the adult mouse hippocampus. Most interestingly, however, depolarizing levels of KCl led to the emergence of a small subpopulation of precursors (approximately eight per hippocampus) with the capacity to generate very large neurospheres (> 250 microm in diameter). Many of these contained cells that displayed the cardinal properties of stem cells: multipotentiality and self-renewal. In contrast, the same conditions led to the opposite effect in the other main neurogenic region of the brain, the subventricular zone, in which neurosphere numbers decreased by approximately 40% in response to depolarizing levels of KCl. Most importantly, we also show that the latent hippocampal progenitor population can be activated in vivo in response to prolonged neural activity found in status epilepticus. This work provides the first direct evidence of a latent precursor and stem cell population in the adult hippocampus, which is able to be activated by neural activity. Because the latent population is also demonstrated to reside in the aged animal, defining the precise mechanisms that underlie its activation may provide a means to combat the cognitive deficits associated with a decline in neurogenesis.

MeSH Terms
Action Potentials/drug effects,physiology Aging/pathology Animals Cell Proliferation/drug effects Cells, Cultured Cognition Disorders/drug therapy,etiology,physiopathology Hippocampus/cytology,physiology Male Mice Mice, Inbred C57BL Mice, Knockout Mice, Transgenic Neuronal Plasticity/drug effects,physiology Neurons/cytology,drug effects,physiology Potassium Chloride/pharmacology Spheroids, Cellular Stem Cells/cytology,drug effects,physiology Synaptic Transmission/drug effects,physiology
Chemicals
Potassium Chloride
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Walker Tara L
Queensland Brain Institute, The University of Queensland, Brisbane, Queensland 4072, Australia.
White Amanda
Black Debra M
Wallace Robyn H
Sah Pankaj
Bartlett Perry F
References (44)
44 references, click to expand
  1. Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway.
    Science. 2001 Oct 12;294(5541):333-9 PMID: 11598293
  2. Excitation-neurogenesis coupling in adult neural stem/progenitor cells.
    Neuron. 2004 May 27;42(4):535-52 PMID: 15157417
  3. Reappearance of hippocampal CA1 neurons after ischemia is associated with recovery of learning and memory.
    J Cereb Blood Flow Metab. 2005 Dec;25(12):1586-95 PMID: 15917746
  4. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation.
    J Neurosci. 1996 Mar 15;16(6):2027-33 PMID: 8604047
  5. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor.
    Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8856-60 PMID: 7568031
  6. p75 neurotrophin receptor expression defines a population of BDNF-responsive neurogenic precursor cells.
    J Neurosci. 2007 May 9;27(19):5146-55 PMID: 17494700
  7. Age-related production of new granule cells in the adult dentate gyrus.
    Neuroreport. 1995 Dec 15;6(18):2479-82 PMID: 8741746
  8. Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis.
    Neuron. 1991 Jul;7(1):165-76 PMID: 1829904
  9. Excitatory amino acid receptors and their role in epilepsy and cerebral ischemia.
    Ann N Y Acad Sci. 1995 May 10;757:492-505 PMID: 7611707
  10. Corticosteroids and hippocampal plasticity.
    Ann N Y Acad Sci. 1994 Nov 30;746:134-42; discussion 142-4, 178-9 PMID: 7825871
  11. Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors.
    J Neurosci. 2002 Mar 1;22(5):1784-93 PMID: 11880507
  12. Regulation of hippocampal neurogenesis in adulthood.
    Biol Psychiatry. 2000 Oct 15;48(8):715-20 PMID: 11063968
  13. BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF.
    Neuron. 1991 Jun;6(6):937-48 PMID: 2054188
  14. Neurogenesis in the adult is involved in the formation of trace memories.
    Nature. 2001 Mar 15;410(6826):372-6 PMID: 11268214
  15. FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain.
    Mol Cell Neurosci. 1995 Oct;6(5):474-86 PMID: 8581317
  16. Increased hippocampal neurogenesis in Alzheimer's disease.
    Proc Natl Acad Sci U S A. 2004 Jan 6;101(1):343-7 PMID: 14660786
  17. Regionally specific and rapid increases in brain-derived neurotrophic factor messenger RNA in the adult rat brain following seizures induced by systemic administration of kainic acid.
    Neuroscience. 1992;47(2):303-15 PMID: 1641125
  18. Programmed cell death of adult-generated hippocampal neurons is mediated by the proapoptotic gene Bax.
    J Neurosci. 2004 Dec 8;24(49):11205-13 PMID: 15590937
  19. De novo generation of neuronal cells from the adult mouse brain.
    Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8591-5 PMID: 1528866
  20. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus.
    J Neurosci. 1997 May 15;17(10):3727-38 PMID: 9133393
  21. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors.
    Cell. 2002 Aug 23;110(4):429-41 PMID: 12202033
  22. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils.
    J Neurosci. 1998 Oct 1;18(19):7768-78 PMID: 9742147
  23. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis.
    Eur J Neurosci. 2003 May;17(10):2042-6 PMID: 12786970
  24. Consequences of pilocarpine-induced recurrent seizures in neonatal rats.
    Brain Dev. 2007 Apr;29(3):157-63 PMID: 17008043
  25. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats.
    J Comp Neurol. 1965 Jun;124(3):319-35 PMID: 5861717
  26. The adult rat hippocampus contains primordial neural stem cells.
    Mol Cell Neurosci. 1997;8(6):389-404 PMID: 9143557
  27. Stroke induces widespread changes of gene expression for glial cell line-derived neurotrophic factor family receptors in the adult rat brain.
    Neuroscience. 2001;106(1):27-41 PMID: 11564414
  28. Neurotransmitters, KCl and antioxidants rescue striatal neurons from apoptotic cell death in culture.
    Brain Res. 1999 Jan 23;816(2):276-85 PMID: 9878784
  29. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system.
    Science. 1992 Mar 27;255(5052):1707-10 PMID: 1553558
  30. Purification of a pluripotent neural stem cell from the adult mouse brain.
    Nature. 2001 Aug 16;412(6848):736-9 PMID: 11507641
  31. Integration of new neurons into functional neural networks.
    J Neurosci. 2006 Nov 22;26(47):12237-41 PMID: 17122048
  32. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia.
    Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):2074-7 PMID: 8446631
  33. Activity-dependent synaptic Wnt release regulates hippocampal long term potentiation.
    J Biol Chem. 2006 Apr 28;281(17):11910-6 PMID: 16501258
  34. Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain.
    Proc Natl Acad Sci U S A. 1983 Apr;80(8):2390-4 PMID: 6572982
  35. "Epileptic" brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies.
    Brain Res Bull. 1983 May;10(5):675-97 PMID: 6871737
  36. Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain.
    Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11879-83 PMID: 8524867
  37. Running enhances neurogenesis, learning, and long-term potentiation in mice.
    Proc Natl Acad Sci U S A. 1999 Nov 9;96(23):13427-31 PMID: 10557337
  38. The adult mouse hippocampal progenitor is neurogenic but not a stem cell.
    J Neurosci. 2005 Nov 23;25(47):10815-21 PMID: 16306394
  39. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone.
    Neuron. 1993 Jul;11(1):173-89 PMID: 8338665
  40. Learning enhances adult neurogenesis in the hippocampal formation.
    Nat Neurosci. 1999 Mar;2(3):260-5 PMID: 10195219
  41. The doublecortin-expressing population in the developing and adult brain contains multipotential precursors in addition to neuronal-lineage cells.
    J Neurosci. 2007 Apr 4;27(14):3734-42 PMID: 17409237
  42. Wnt signalling regulates adult hippocampal neurogenesis.
    Nature. 2005 Oct 27;437(7063):1370-5 PMID: 16251967
  43. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants.
    Science. 2003 Aug 8;301(5634):805-9 PMID: 12907793
  44. Hippocampal damage and kainic acid injection induce a rapid increase in mRNA for BDNF and NGF in the rat brain.
    Exp Neurol. 1991 Oct;114(1):35-43 PMID: 1915733
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2008-05-14
Pages
5240-7
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6670644
Subset
IM
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